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Fluoroquinolone-resistant Campylobacter in animal reservoirs: dynamics of development, resistance mechanisms and ecological fitness

Published online by Cambridge University Press:  28 February 2007

Qijing Zhang ,
Jun Lin  and
Sonia Pereira
Qijing Zhang*
Affiliation:
Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, IA, USA
Jun Lin
Affiliation:
Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, IA, USA
Sonia Pereira
Affiliation:
Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, IA, USA
*
*Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, 1116 Veterinary Medicine Bldg., Ames, IA 50011, USA E-mail: [email protected]
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Abstract

Thermophilic Campylobacter species, including Campylobacter jejuni and Campylobacter coli, are responsible for foodborne campylobacteriosis in humans and are increasingly resistant to fluoroquinolone (FQ) antimicrobials. The therapeutic use of FQ antimicrobial agents in food animal production, particularly in poultry, has become a concern for public health, because the practice may promote the emergence of FQ-resistant Campylobacter that can be transmitted to humans through the food chain. Recent studies have indicated that Campylobacter displays a hypermutable phenotype in response to in vivo treatment with FQ antimicrobials, resulting in the rapid emergence of resistant mutants. Distinct from other Gram-negative bacteria, the acquisition of FQ resistance in Campylobacter does not require stepwise accumulation of gyrA mutations and overexpression of efflux pumps, and is mainly mediated by single-step point mutations in gyrA in the presence of a constitutively expressed multidrug efflux pump, CmeABC. The simplicity of the resistance mechanisms may facilitate the rapid adaptation of Campylobacter to FQ treatment. The FQ-resistant Campylobacter mutants derived from chickens do not show a fitness cost in vivo and are ecologically competitive in the colonization of chickens even in the absence of antimicrobial selection pressure. These findings suggest that FQ-resistant Campylobacter may continue to persist regardless of antimicrobial usage, and highlight the need for extra effort to prevent the occurrence and spread of FQ-resistant Campylobacter in animal reservoirs.

Keywords

fluoroquinoloneantimicrobialantibioticCampylobacterresistancepoultry
Type
Research Article
Information
Animal Health Research Reviews , Volume 4 , Issue 2 , December 2003 , pp. 63 - 72
Copyright
Copyright © CAB International 2003

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References

Aarestrup, FM and Wegener, HC (1999). The effects of antibiotic usage in food animals on the development of antimicrobial resistance of importance for humans in Campylobacter and Escherichia coli. Microbes and Infection 1: 639–644.CrossRefGoogle ScholarPubMed
Aarestrup, FM, Bager, F, Jensen, NE, Madsen, M, Meyling, A and Wegener, HC (1998). Surveillance of antimicrobial resistance in bacteria isolated from food animals to antimicrobial growth promoters and related therapeutic agents in Denmark. Acta Pathologica, Microbiologica, et Immunologica Scandinavica 106: 606–622.CrossRefGoogle ScholarPubMed
Altekruse, SF, Stern, NJ, Fields, PI and Swerdlow, DL (1999). Campylobacter jejuni —an emerging foodborne pathogen. Emerging Infectious Diseases 5: 28–35.CrossRefGoogle ScholarPubMed
Andersson, DI and Levin, BR (1999). The biological cost of antibiotic resistance. Current Opinion in Microbiology 2: 489–493.CrossRefGoogle ScholarPubMed
Appelbaum, PC and Hunter, PA (2000). The fluoroquinolone antibacterials: past, present and future perspectives. International Journal of Antimicrobial Agents 16: 5–15.CrossRefGoogle ScholarPubMed
Bachoual, R, Ouabdesselam, S, Mory, F, Lascols, C, Soussy, CJ and Tankovic, J (2001). Single or double mutational alterations of gyrA associated with fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli. Microbial Drug Resistance 7: 257–261.CrossRefGoogle ScholarPubMed
Beery, JT, Hugdahl, MB and Doyle, MP (1988). Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Applied and Environmental Microbiology 54: 2365–2370.CrossRefGoogle ScholarPubMed
Bjorkman, J, Hughes, D and Andersson, DI (1998). Virulence of antibiotic-resistant Salmonella typhimurium. Proceedings of the National Academy of Sciences of the United States of America 95: 3949–3953.CrossRefGoogle ScholarPubMed
Bjorkman, J, Nagaev, I, Berg, OG, Hughes, D and Andersson, DI (2000). Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287: 1479–1482.CrossRefGoogle ScholarPubMed
Bjorkholm, B, Sjolund, M, Falk, PG, Berg, OG, Engstrand, L and Andersson, DI (2001). Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proceedings of the National Academy of Sciences of the United States of America 98: 14607–14612.CrossRefGoogle ScholarPubMed
Blaser, MJ (1997). Epidemiologic and clinical features of Campylobacter jejuni infections. Journal of Infectious Diseases 176 (Suppl. 2): S103–S105.CrossRefGoogle ScholarPubMed
Carattoli, A, Dionisi, A and Luzzi, I (2002). Use of a LightCycler gyrA mutation assay for identification of ciprofloxacin-resistant Campylobacter coli. FEMS Microbiology Letters 214: 87–93.CrossRefGoogle ScholarPubMed
Chu, DT (1999). Recent progress in novel macrolides, quinolones, and 2-pyridones to overcome bacterial resistance. Medicinal Research Reviews 19: 497–520.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Cooper, R, Segal, H, Lastovica, AJ and Elisha, BG (2002). Genetic basis of quinolone resistance and epidemiology of resistant and susceptible isolates of porcine Campylobacter coli strains. Journal of Applied Microbiology 93: 241–249.CrossRefGoogle ScholarPubMed
Drlica, K and Malik, M (2003). Fluoroquinolones: action and resistance. Current Topics in Medicinal Chemistry 3: 249–282.CrossRefGoogle ScholarPubMed
Drlica, K and Zhao, X (1997). DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiology and Molecular Biology Reviews 61: 377–392.Google ScholarPubMed
Ellis-Pegler, RB, Hyman, LK, Ingram, RJ and McCarthy, M (1995). A placebo controlled evaluation of lomefloxacin in the treatment of bacterial diarrhoea in the community. Journal of Antimicrobial Chemotherapy 36: 259–263.CrossRefGoogle ScholarPubMed
Engberg, J, Aarestrup, FM, Taylor, DE, Gerner-Smidt, P and Nachamkin, I (2001). Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerging Infectious Diseases 7: 24–34.CrossRefGoogle Scholar
Friedman, CR, Neimann, J, Wegener, HC and Tauxe, RV (2000) Epidemiology of C. jejuni infections in the United States and other industrialized nations. In: Nachamkin, I and Blaser, MJ (editors). Campylobacter. Washington, DC: ASM Press, pp. 121–138.Google Scholar
Ge, B, Bodeis, S, Walker, RD, White, DG, Zhao, S, McDermott, PF and Meng, J (2002). Comparison of the Etest and agar dilution for in vitro antimicrobial susceptibility testing of Campylobacter. Journal of Antimicrobial Chemotherapy 50: 487–494.CrossRefGoogle ScholarPubMed
Ge, B, White, DG, McDermott, PF, Girard, W, Zhao, S, Hubert, S and Meng, J (2003). Antimicrobial-resistant Campylobacter species from retail raw meats. Applied and Environmental Microbiology 69: 3005–3007.CrossRefGoogle ScholarPubMed
Gebreyes, WA, Bahnson, PB, Funk, JA, Morrow, WE and Thakur, S (2003) Antimicrobial resistance and diversity of Campylobacter in antimicrobial free and conventionally reared market swine. Abstracts of the International Workshop on Campylobacter, Helicobacter and Related Organisms, 12th meeting, Aarhus, Denmark (Suppl.) p.1.Google Scholar
Gibreel, A, Sjogren, E, Kaijser, B, Wretlind, B and Skold, O (1998). Rapid emergence of high-level resistance to quinolones in Campylobacter jejuni associated with mutational changes in gyrA and parC. Antimicrobial Agents and Chemotherapy 42: 3276–3278.CrossRefGoogle ScholarPubMed
Gillespie, SH, Voelker, LL and Dickens, A (2002). Evolutionary barriers to quinolone resistance in Streptococcus pneumoniae. Microbial Drug Resistance 8: 79–84.CrossRefGoogle ScholarPubMed
Gootz, TD and Martin, BA (1991). Characterization of high-level quinolone resistance in Campylobacter jejuni. Antimicrobial Agents and Chemotherapy 35: 840–845.CrossRefGoogle ScholarPubMed
Hayward, CL, Erwin, ME, Barrett, MS and Jones, RN (1999). Comparative antimicrobial activity of gatifloxacin tested against Campylobacter jejuni including fluoroquinolone-resistant clinical isolates. Diagnostic Microbiology and Infectious Disease 34: 99–102.CrossRefGoogle ScholarPubMed
Hooper, DC (1998). Clinical applications of quinolones. Biochimica et Biophysica Acta 1400: 45–61.CrossRefGoogle ScholarPubMed
Hooper, DC (2001). Emerging mechanisms of fluoroquinolone resistance. Emerging Infectious Diseases 7: 337–341.CrossRefGoogle ScholarPubMed
Huang, MB, Baker, CN, Banerjee, S and Tenover, FC (1992). Accuracy of the E test for determining antimicrobial susceptibilities of staphylococci, enterococci, Campylobacter jejuni, and gram-negative bacteria resistant to antimicrobial agents. Journal of Clinical Microbiology 30: 3243–3248.CrossRefGoogle Scholar
Jacobs-Reitsma, WF, Kan, CA and Bolder, NM (1994). The induction of quinolone resistance in Campylobacter bacteria in broilers by quinolone treatment. Letters in Applied Microbiology 19: 228–231.CrossRefGoogle Scholar
Levin, BR, Perrot, V and Walker, N (2000). Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154: 985–997.CrossRefGoogle ScholarPubMed
Lin, J, Michel, LO and Zhang, Q (2002). CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrobial Agents and Chemotherapy 46: 2124–2131.CrossRefGoogle ScholarPubMed
Lin, J, Sahin, O, Michel, LO and Zhang, Q (2003). Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infection and Immunity 71: 4250–4259.CrossRefGoogle ScholarPubMed
Luber, P, Bartelt, E, Genschow, E, Wagner, J and Hahn, H (2003). Comparison of broth microdilution, E test, and agar dilution methods for antibiotic susceptibility testing of Campylobacter jejuni and Campylobacter coli. Journal of Clinical Microbiology 41: 1062–1068.CrossRefGoogle ScholarPubMed
Luo, N, Sahin, O, Lin, J, Michel, LO and Zhang, Q (2003a). In vivo selection of Campylobacter isolates with high levels of fluoroquinolone resistance associated with gyrA mutations and the function of the CmeABC efflux pump. Antimicrobial Agents and Chemotherapy 47: 390–394.CrossRefGoogle ScholarPubMed
Luo, N, Sahin, O, Lin, J and Zhang, Q (2003b) Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Abstracts of the 2003 Annual Conference on Antimicrobial Resistance, National Foundation for Infectious Disease, Bethesda, Maryland p. 35(S21).Google Scholar
McDermott, PF, Bodeis, SM and Walker, RD (2001) Development of standardized antimicrobial susceptibility testing for Campylobacter jejuni. Abstracts of the International Workshop on Campylobacter, Helicobacter and Related Organisms, 11th meeting, Freiburg, Germany p.109.Google Scholar
McDermott, PF, Bodeis, SM, English, LL, White, DG, Walker, RD, Zhao, S, Simjee, S and Wagner, DD (2002). Ciprofloxacin resistance in Campylobacter jejuni evolves rapidly in chickens treated with fluoroquinolones. Journal of Infectious Diseases 185: 837–840.CrossRefGoogle ScholarPubMed
McEwen, SA, Fedorka-Cray, PJ (2002). Antimicrobial use and resistance in animals. Clinical Infectious Disease 34 (Suppl. 3): S93–S106.CrossRefGoogle ScholarPubMed
Mead, PS, Slutsker, L, Dietz, V, McCaig, LF, Bresee, JS, Shapiro, C, Griffin, PM and Tauxe, RV (1999). Food-related illness and death in the United States. Emerging Infectious Diseases 5: 607–625.CrossRefGoogle ScholarPubMed
Meinersmann, RJ, Rigsby, WE, Stern, NJ, Kelley, LC, Hill, JE and Doyle, MP (1991). Comparative study of colonizing and noncolonizing Campylobacter jejuni. American Journal of Veterinary Research 52: 1518–1522.CrossRefGoogle ScholarPubMed
Nachamkin, I, Ung, H and Li, M (2002). Increasing fluoroquinolone resistance in Campylobacter jejuni, Pennsylvania, USA, 1982–2001, Emerging Infectious Diseases 8: 1501–1503.CrossRefGoogle ScholarPubMed
Nagaev, I, Bjorkman, J, Andersson, DI and Hughes, D (2001). Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus. Molecular Microbiology 40: 433–439.CrossRefGoogle ScholarPubMed
NCCLS (2002). Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Approved standards M31–A2. Villanova (PA): National Committee for Clinical Laboratory Standards.Google Scholar
Newell, DG and Wagenaar, JA (2000) Poultry infections and their control at the farm level. In: Nachamkin, I and Blaser, MJ (editors). Campylobacter Washington, DC: ASM Press pp. 497–509.Google Scholar
Norby, B, Bartlett, P and Kaneene, J (2003) Prevalence and antimicrobial susceptibility of Campylobacter in antibiotic-free and conventional swine farms in the Mid-Western United States. Abstracts of the International Workshop on Campylobacter, Helicobacter and Related Organisms, 12th meeting, Aarhus, Denmark, p53.Google Scholar
Normark, BH and Normark, S (2002). Evolution and spread of antibiotic resistance. Journal of Internal Medicine 252: 91–106.CrossRefGoogle ScholarPubMed
Oncul, O, Zarakolu, P, Oncul, O and Gur, D (2003). Antimicrobial susceptibility testing of Campylobacter jejuni: a comparison between Etest and agar dilution method. Diagnostic Microbiology and Infectious Disease 45: 69–71.CrossRefGoogle ScholarPubMed
Parkhill, J, Wren, BW, Mungall, K, Ketley, JM, Churcher, C, Basham, D, Chillingworth, T, Davies, RM, Feltwell, T, Holroyd, S, Jagels, K, Karlyshev, AV, Moule, S, Pallen, MJ, Penn, CW, Quail, MA, Rajandream, MA, Rutherford, KM van Vliet, AH, Whitehead, S and Barrell, BG (2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665–668.CrossRefGoogle ScholarPubMed
Payot, S, Cloeckaert, A and Chaslus-Dancla, E (2002). Selection and characterization of fluoroquinolone-resistant mutants of Campylobacter jejuni using enrofloxacin. Microbial Drug Resistance 8: 335–343.CrossRefGoogle ScholarPubMed
Pedersen, K and Wedderkopp, A (2003). Resistance to quinolones in Campylobacter jejuni and Campylobacter coli from Danish broilers at farm level. Journal of Applied Microbiology 94: 111–119.CrossRefGoogle ScholarPubMed
Pezzotti, G, Serafin, A, Luzzi, I, Mioni, R, Milan, M and Perin, R (2003). Occurrence and resistance to antibiotics of Campylobacter jejuni and Campylobacter coli in animals and meat in northeastern Italy. International Journal of Food Microbiology 82: 281–287.CrossRefGoogle ScholarPubMed
Piddock, LJ (1995). Quinolone resistance and Campylobacter spp. Journal of Antimicrobial Chemotherapy 36: 891–898.CrossRefGoogle ScholarPubMed
Piddock, LJ, Ricci, V, Pumbwe, L, Everett, MJ and Griggs, DJ (2003). Fluoroquinolone resistance in Campylobacter species from man and animals: detection of mutations in topoisomerase genes. Journal of Antimicrobial Chemotherapy 51: 19–26.CrossRefGoogle ScholarPubMed
Poole, K (2000). Efflux-mediated resistance to fluoroquinolones in gram-negative bacteria. Antimicrobial Agents and Chemotherapy 44: 2233–2241.CrossRefGoogle ScholarPubMed
Pumbwe, L and Piddock, LJ (2002). Identification and molecular characterisation of CmeB, a Campylobacter jejuni multidrug efflux pump. FEMS Microbiology Letters 206: 185–189.CrossRefGoogle ScholarPubMed
Rautelin, H, Renkonen, OV and Kosunen, TU (1991). Emergence of fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli in subjects from Finland. Antimicrobial Agents and Chemotherapy 35: 2065–2069.CrossRefGoogle Scholar
Ruiz, J, Goni, P, Marco, F, Gallardo, F, Mirelis, B, Jimenez de Anta, T and Vila, J (1998). Increased resistance to quinolones in Campylobacter jejuni: a genetic analysis of gyrA gene mutations in quinolone-resistant clinical isolates. Microbiology and Immunology 42: 223–226.CrossRefGoogle ScholarPubMed
Saenz, Y, Zarazaga, M, Lantero, M, Gastanares, MJ, Baquero, F and Torres, C (2000). Antibiotic resistance in Campylobacter strains isolated from animals, foods, and humans in Spain in 1997–1998. Antimicrobial Agents and Chemotherapy 44: 267–271.CrossRefGoogle ScholarPubMed
Sahin, O, Morishita, TY and Zhang, Q (2002). Campylobacter colonization in poultry: sources of infection and modes of transmission. Animal Health Research Reviews 3: 95–105.CrossRefGoogle ScholarPubMed
Sahin, O, Zhang, Q and Morishita, TY (2003) Detection of Campylobacter. In: Torrence, ME and Isaacson, RE (editors). Microbial Food Safety in Animal Agriculture. Ames (IA): Iowa State Press, pp. 183–193.Google Scholar
Sanchez, R, Fernandez-Baca, V, Diaz, MD, Munoz, P, Rodriguez-Creixems, M, and Bouza, E (1994). Evolution of susceptibilities of Campylobacter spp. to quinolones and macrolides. Antimicrobial Agents and Chemotherapy 38: 1879–1882.CrossRefGoogle ScholarPubMed
Sander, P, Springer, B, Prammananan, T, Sturmfels, A, Kappler, M, Pletschette, M and Bottger, EC (2002). Fitness cost of chromosomal drug resistance-conferring mutations. Antimicrobial Agents and Chemotherapy 46: 1204–1211.CrossRefGoogle ScholarPubMed
Segreti, J, Gootz, TD, Goodman, LJ, Parkhurst, GW, Quinn, JP, Martin, BA and Trenholme, GM (1992). High-level quinolone resistance in clinical isolates of Campylobacter jejuni. Journal of Infectious Diseases 165: 667–670.CrossRefGoogle ScholarPubMed
Shea, ME and Hiasa, H (1999). Interactions between DNA helicases and frozen topoisomerase IV-quinolone-DNA ternary complexes. Journal of Biological Chemistry 274: 22747–22754.CrossRefGoogle ScholarPubMed
Silley, P (2003). Campylobacter and fluoroquinolones: a bias data set? Environmental Microbiology 5: 219–230.CrossRefGoogle ScholarPubMed
Slutsker, L, Altekruse, SF and Swerdlow, DL (1998). Foodborne diseases: emerging pathogens and trends. Infectious Disease Clinics of North America 12: 199–216.CrossRefGoogle ScholarPubMed
Smith, KE, Besser, JM, Hedberg, CW, Leano, FT, Bender, JB, Wicklund, JH, Johnson, BP, Moore, KA and Osterholm, MT (1999). Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992–1998. New England Journal of Medicine 340: 1525–1532.CrossRefGoogle ScholarPubMed
Smith, KE, Bender, JB and Osterholm, MT (2000) Antimicrobial resistance in animals and relevance to human infections. In: Nachamkin, I and Blaser, MJ (editors). Campylobacter. Washington, DC: ASM Press, pp. 483–495.Google ScholarPubMed
Stern, NJ, Clavero, MR, Bailey, JS, Cox, NA and Robach, MC (1995). Campylobacter spp. in broilers on the farm and after transport. Poultry Science 74: 937–941.CrossRefGoogle ScholarPubMed
Tauxe, RV (2002). Emerging foodborne pathogens. International Journal of Food Microbiology 78: 31–41.CrossRefGoogle ScholarPubMed
Trieber, CA and Taylor, DE (2000) Mechanisms of antibiotic resistance in Campylobacter. In: Nachamkin, I and Blaser, MJ (editors). Campylobacter. Washington, DC: ASM Press pp. 441–454.Google Scholar
Van Looveren, M, Daube, G, De Zutter, L, Dumont, JM, Lammens, C, Wijdooghe, M, Vandamme, P, Jouret, M, Cornelis, M and Goossens, H (2001). Antimicrobial susceptibilities of Campylobacter strains isolated from food animals in Belgium. Journal of Antimicrobial Chemotherapy 48: 235–240.CrossRefGoogle ScholarPubMed
Wang, Y, Huang, WM and Taylor, DE (1993). Cloning and nucleotide sequence of the Campylobacter jejuni gyrA gene and characterization of quinolone resistance mutations. Antimicrobial Agents and Chemotherapy 37: 457–463.CrossRefGoogle ScholarPubMed
Wempe, JM, Genigeorgis, CA, Farver, TB and Yusufu, HI (1983). Prevalence of Campylobacter jejuni in two California chicken processing plants. Applied and Environmental Microbiology 45: 355–359.CrossRefGoogle ScholarPubMed
White, DG, Zhao, S, Simjee, S, Wagner, DD and McDermott, PF (2002). Antimicrobial resistance of foodborne pathogens. Microbes and Infection 4: 405–412.CrossRefGoogle ScholarPubMed
Willis, WL and Murray, C (1997). Campylobacter jejuni seasonal recovery observations of retail market broilers. Poultry Science 76: 314–317.CrossRefGoogle ScholarPubMed
Willmott, CJ, Critchlow, SE, Eperon, IC and Maxwell, A (1994). The complex of DNA gyrase and quinolone drugs with DNA forms a barrier to transcription by RNA polymerase. Journal of Molecular Biology 242: 351–363.CrossRefGoogle ScholarPubMed
Wilson, DL, Abner, SR, Newman, TC, Mansfield, LS and Linz, JE (2000). Identification of ciprofloxacin-resistant Campylobacter jejuni by use of a fluorogenic PCR assay. Journal of Clinical Microbiology 38: 3971–3978.CrossRefGoogle ScholarPubMed
Wretlind, B, Stromberg, A, Ostlund, L, Sjogren, E and Kaijser, B (1992). Rapid emergence of quinolone resistance in Campylobacter jejuni in patients treated with norfloxacin. Scandinavian Journal of Infectious Diseases 24: 685–686.CrossRefGoogle ScholarPubMed
Zirnstein, G, Li, Y, Swaminathan, B and Angulo, F (1999). Ciprofloxacin resistance in Campylobacter jejuni isolates: detection of gyrA resistance mutations by mismatch amplification mutation assay PCR and DNA sequence analysis. Journal of Clinical Microbiology 37: 3276–3280.CrossRefGoogle ScholarPubMed
Zirnstein, G, Helsel, L, Li, Y, Swaminathan, B and Besser, J (2000). Characterization of gyrA mutations associated with fluoroquinolone resistance in Campylobacter coli by DNA sequence analysis and MAMA PCR. FEMS Microbiology Letters 190: 1–7.CrossRefGoogle ScholarPubMed